State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I

Abstract

Plants and green algae optimize photosynthesis in changing light conditions by balancing the amount of light absorbed by photosystems I and II. These photosystems work in series to extract electrons from water and reduce NADP + to NADPH. Light-harvesting complexes (LHCs) are held responsible for maintaining the balance by moving from one photosystem to the other in a process called state transitions. In the green alga Chlamydomonas reinhardtii, a photosynthetic model organism, state transitions are thought to involve 80% of the LHCs. Here, we demonstrate with picosecond-fluorescence spectroscopy on C. reinhardtii cells that, although LHCs indeed detach from photosystem II in state 2 conditions, only a fraction attaches to photosystem I. The detached antenna complexes become protected against photodamage via shortening of the excited-state lifetime. It is discussed how the transition from state 1 to state 2 can protect C. reinhardtii in high-light conditions and how this differs from the situation in plants.time-resolved fluorescence spectroscopy | photoprotection O xygenic photosynthesis is the most important process for fueling life on earth. Light capture and subsequent charge separation processes occur in the so-called photosystems I and II (PSI and PSII). In plants and green algae, both PSs consist of a pigment-protein core complex surrounded by outer light-harvesting complexes (LHCs). Electronic excitations induced by the absorption of sunlight lead to charge separation in the reaction centers (RCs) of PSI and PSII, located in the cores of the PSs. These PSs work in series to extract electrons from water and reduce NADP + to NADPH. For optimal linear electron transport from water to NADP + , a balance is needed for the amount of light absorbed by the pigments in the two PSs.Besides carotenoids, the PSII core contains 35 chlorophylls a (Chls a), whereas this number is close to 100 for PSI (1). The outer LHCs consist of various components: The major lightharvesting complex LHCII (a trimer) harbors 12 carotenoids (Cars) and 42 chlorophylls (Chls), 24 of which are Chls a (2), the pigments that are largely responsible for excitation energy transfer (EET) to the PSII RC. In higher plants, there are also three monomeric minor LHCs per core, called CP24, CP26, and CP29, which show high sequence homology with LHCII (see, e.g., ref.3). In nonstressed conditions, between 85% and 90% of the excitations in PSII lead to charge separation in the RC (4). PSI in plants binds four LHCs (Lhca1-4) (5). The amount of LHCII in the plant membranes is variable and usually ranges from approximately two to approximately four trimers per PSII core, most of which are functionally connected to PSII, although part is also associated with PSI (6). In Chlamydomonas reinhardtii, PSI antenna size differs and there are nine Lhcas per PSI (7). Nine LhcbM genes, plus CP29 and CP26, codify for the antenna complexes of PSII (8), and it was recently shown that, in addition to CP26 and CP29, the PSII supercomplex contains three LHCII trimers per m...

The High Efficiency of Photosystem I in the Green Alga Chlamydomonas reinhardtii Is Maintained after the Antenna Size Is Substantially Increased by the Association of Light-harvesting Complexes II

“…If a large population of PSI-LHCI-LHCII particles should be expected in the cells in state 2 as compared with state 1, not only a large difference in the amplitude of the PSI component should be observed but also a significant difference in its lifetime. The fact that none of these effects were observed in the time-resolved measurements in the cells indicates that the difference in the amount of LHCII associated with PSI in state 1 and 2 is relatively small as concluded by Ü nlü et al (27). The detailed modeling of the measurements (Fig.…”

“…The presence of seven Lhcbs slows down the overall trapping by 15 ps at 400 nm and by 27 ps at 475 nm excitation (Table 2). This result helps in interpreting the time-resolved data on C. reinhardtii in vivo (27). If a large population of PSI-LHCI-LHCII particles should be expected in the cells in state 2 as compared with state 1, not only a large difference in the amplitude of the PSI component should be observed but also a significant difference in its lifetime.…”

“…29); however, recent results suggest that the mechanism and probably also the physiological role of this process are different from in plants. It was indeed observed that although a large part of LHCII functionally disconnects from PSII during the state 1 to state 2 transition, only part of it associates with PSI, whereas the rest gets quenched (27,28,30). However, due to the complexity of the cells and the presence of different LHCII pools, a conclusion about excitation energy transfer efficiency from Lhcbs to PSI could not be made.…”

Induction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii

“…Because state 2 facilitates induction of PSII activity in the absence of hydrogenase , we propose that the increase of PSI antenna size upon state 2 might enhance PSI-CEF rate (Cardol et al, 2009;Alric, 2010Alric, , 2014 and therefore promote ATP synthesis and CBB cycle activity. Nevertheless, the attachment of LHCII to PSI in state 2 has been recently called into question (Nagy et al, 2014;Ünlü et al, 2014). In this .…”

STATE TRANSITION7-Dependent Phosphorylation Is Modulated by Changing Environmental Conditions, and Its Absence Triggers Remodeling of Photosynthetic Protein Complexes

“…The proportion of mobile LHCII antenna is about 80% in the alga, whereas in Arabidopsis, only 15% to 20% of LHCII is transferred to PSI under state 2 conditions . However, the large increase in PSI antenna size in C. reinhardtii has recently been challenged (Nagy et al, 2014;Ünlü et al, 2014): while 70% to 80% of mobile LHCII detached from PSII in response to transition to state 2 conditions, only a fraction of about 20% functionally attached to PSI.…”